Organ preformation in overwintering buds of perennial plants has been known for almost two centuries. It is hypothesized to underlie fast growth and early flowering, but its frequency, phylogenetic distribution, and ecological relevance have never been systematically examined. We microscopically observed inflorescence preformation in overwintering buds (IPB) in the autumn. We studied a phylogenetically and ecologically representative set of 330 species of temperate perennial angiosperms and linked these observations with quantitative data on species' flowering phenology, genome size, and ecology. IPB was observed in 34% of species examined (in 14% species the stamens and/or pistils were already developed). IPB is fairly phylogenetically conserved and frequent in many genera (Alchemilla, Carex, Euphorbia, Geranium, Primula, Pulmonaria) or families (Ranunculaceae, Euphorbiaceae, Violaceae, Boraginaceae). It was found in species of any genome size, although it was almost universal in those with large genomes. Compared with non-IPB species, IPB species flowered 38 d earlier on average and were more common in shaded and undisturbed habitats. IPB is a surprisingly widespread adaptation for early growth in predictable (undisturbed) conditions. It contributes to temporal niche differentiation and has important consequences for understanding plant phenology, genome size evolution, and phylogenetic structure of plant communities.

Department of Botany and Zoology Faculty of Science Masaryk University Brno 611 37 Czech Republic

Department of Botany Faculty of Science Charles University Praha 2 128 43 Czech Republic

Department of Functional Ecology Institute of Botany of the Czech Academy of Sciences Třeboň 379 01 Czech Republic

Department of Population Ecology Institute of Botany of the Czech Academy of Sciences Průhonice 252 43 Czech Republic

Institute of Wetland Ecology and Clone Ecology Taizhou University Taizhou 318000 China

Zobrazit více v PubMed

Aarssen L. 2008. Death without sex - the 'problem of the small' and selection for reproductive economy in flowering plants. Evolutionary Ecology 22: 279-298.

Albani MC, Coupland G. 2010. Comparative analysis of flowering in annual and perennial plants. Current Topics in Developmental Biology. 91: 323-348.

Austen EJ, Rowe L, Stinchcombe JR, Forrest JRK. 2017. Explaining the apparent paradox of persistent selection for early flowering. New Phytologist 215: 929-934.

Aydelotte AR, Diggle PK. 1997. Analysis of developmental preformation in the alpine herb Caltha leptosepala (Ranunculaceae). American Journal of Botany 84: 1646-1657.

Beaulieu JM, Leitch IJ, Patel S, Pendharkar A, Knight CA. 2008. Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytologist 179: 975-986.

Bennett MD. 1987. Variation in genomic form in plants and its ecological implications. New Phytologist 106: 177-200.

Bommert P, Whipple C. 2018. Grass inflorescence architecture and meristem determinacy. Seminars in Cell and Developmental Biology 79: 37-47.

Bucher SF, Konig P, Menzel A, Migliavacca M, Ewald J, Romermann C. 2018. Traits and climate are associated with first flowering day in herbaceous species along elevational gradients. Ecology and Evolution 8: 1147-1158.

CaraDonna PJ, Bain JA. 2016. Frost sensitivity of leaves and flowers of subalpine plants is related to tissue type and phenology. Journal of Ecology 104: 55-64.

Christensen RHB. 2018. ordinal - regression models for ordinal data. R package v.2018.4-19. [WWW document] URL http://www.cran.r-project.org/package=ordinal/

Crawley MJ, Long CR. 1995. Alternate bearing, predator satiation and seedling recruitment in Quercus robur L. Journal of Ecology 83: 683-696.

Dafni A, Cohen D, Noy-Meir I. 1981. Life-cycle variation in geophytes. Annals of the Missouri Botanical Garden 68: 652-660.

Diekmann M. 2003. Species indicator values as an important tool in applied plant ecology - a review. Basic and Applied Ecology 4: 493-506.

Diggle PK. 1997. Extreme preformation in alpine Polygonum viviparum: an architectural and developmental analysis. American Journal of Botany 84: 154-169.

Durka W, Michalski SG. 2012. Daphne: a dated phylogeny of a large European flora for phylogenetically informed ecological analyses. Ecology 93: 2297.

Edwards EJ, Chatelet DS, Chen B-Ch, Ong JY, Tagane Sh, Kanemitsu H, Tagawa K, Teramoto K, Park B, Chung K-F et al. 2017. Convergence, consilience, and the evolution of temperate deciduous forests. American Naturalist 190: S87-S104.

Ehrlén J. 2015. Selection on flowering time in a life-cycle context. Oikos 124: 92-101.

Ehrlén J, van Groenendael J. 2001. Storage and the delayed costs of reproduction in the understorey perennial Lathyrus vernus. Journal of Ecology 89: 237-246.

Ellenberg H, Weber HE, Düll R, Wirth V, Werner W, Paulißen D. 1992. Zeigerwerte von pflanzen in mitteleuropa. In: Scripta Geobotanica 18. Göttingen, Germany: Goltze.

Foerste AF. 1891. On the formation of the flower buds of spring-blossoming plants during the preceding summer. Bulletin of the Torrey Botanical Club 18: 101-106.

Freckleton RP, Harvey PH, Pagel M. 2002. Phylogenetic analysis and comparative data: a test and review of evidence. American Naturalist 160: 712-726.

Geber MA, de Kroon H, Watson MA. 1997a. Organ preformation in mayapple as a mechanism for historical effects on demography. Journal of Ecology 85: 211-223.

Geber MA, Watson MA, de Kroon H. 1997b. Organ preformation, development, and resource allocation in perennials. In: Bazzaz FA, Grace J, eds. Plant resource allocation. San Diego, CA, USA: Academic Press, 113-141.

Geiger R, Aron R, Todhunter P. 2009. The climate near the ground, 7thedn. Lanham, MD, USA: Rowman & Littlefield.

Götzenberger L, de Bello F, Brathen KA, Davison J, Dubuis A, Guisan A, Lindborg R, Moora M, Pärtel M et al. 2012. Ecological assembly rules in plant comminities-approaches, patterns and prospects. Biological Reviews 87: 111-127.

Greilhuber J, Doležel J, Lysák MA, Bennett MD. 2005. The origin, evolution and proposed stabilization of the terms 'genome size' and 'C-value' to describe nuclear DNA contents. Annals of Botany 95: 255-260.

Grime JP. 1983. Prediction of weed and crop response to climate based upon measurements of nuclear DNA content. Aspect of Applied Biology 4: 87-98.

Grime JP, Mowforth MA. 1982. Variation in genome size - an ecological interpretation. Nature 299: 151-153.

Guédon Y, Puntieri JG, Sabatier S, Barthélémy D. 2006. Relative extents of preformation and neoformation in tree shoots: analysis by a deconvolution method. Annals of Botany 98: 835-844.

Harmon LJ, Weir JT, Brock ChD, Glor RE, Challenger W. 2008. Geiger: investigating evolutionary radiations. Phylogenetics 24: 129-131.

Hegnauer R. 1964. Chemotaxonomie der Pflanzen: Eine Übersicht über die Verbreitung und die systematische Bedeutung der Pflanzenstoffe. Band 3: Dicotyledoneae: Acanthaceae-Cyrillaceae. Basel, Switzerland: Birkhäuser.

Herben T, Chytrý M, Klimešová J. 2016. A quest for species-level indicator values for disturbance. Journal of Vegetation Science 27: 628-636.

Huang L, Koubek T, Weiser M, Herben T. 2018. Environmental drivers and phylogenetic constraints of growth phenologies across a large set of herbaceous species. Journal of Ecology 106: 1621-1633.

Huber H, Whigham DF, O’Neill J. 2004. Timing of disturbance changes the balance between growth and survival of parent and offspring ramets in the clonal forest undersstorey herb Uvularia perfoliata. Evolutionary Ecology 18: 521-539.

Iler AM, Compagnoni A, Inouye DW, Williams J, CaraDonna PJ, Anderson A, Miller TEX. 2019. Reproductive losses due to climate change-induced earlier flowering are not the primary threat to plant popuplation variability in a perennial herb. Journal of Ecology 107: 1931-1943.

Inouye DW. 1986. Long-term preformation of leaves and inflorescences by a long-lived perennial monocarp, Frasera speciosa (Gentianaceae). American Journal of Botany 73: 1535-1540.

Irmisch T. 1850. Zur Morphologie der Monokotylischen Knollen und Zwiebelgewächse. Berlin, Germany: G. Reimer.

Jones CS, Watson MA. 2001. Heteroplasty and preformation in mayapple, Podophyllum peltatum (Berberidaceae): developmental flexibility and morphological constraint. American Journal of Botany 88: 1340-1358.

Kamenetsky R, Zaccai M, Flaishman MA. 2013. Florogenesis. In: Kamenetsky R, Okubo H, eds. Ornamental geophytes. Boca Raton, FL, USA: CRC Press, 197-232.

Klimešová J, Danihelka J, Chrtek J, de Bello F, Herben T. 2017. CLO-PLA: a database of clonal and bud-bank traits of the central European flora. Ecology 98: 1179.

Klimešová J, Klimeš L. 2008. Clonal growth and bud banks of plants in the Czech flora: an evaluation using the CLO-PLA3 database. Preslia 80: 255-275.

Körner Ch, Riedl S, Keplinger T, Richter A, Wiesenbauer J, Achweingruber F, Hiltbrunner E. 2019. Life at 0 °C: the biology of the alpine snowbed plant Soldanella pusilla. Alpine Botany 129: 63-80.

Kozhevnikov AB. 1931. On overwintering and development of spring plants of lime forest. Byulleten Moskovskogo Obschchestva Ispytateley Prirody, Otdel Biologicheskiy 1-2: 79-108.

Ladinig U, Hacker J, Neuner G, Wagner J. 2013. How endangered is sexual reproduction of high-mountain plants by summer frosts? Frost resistance, frequency of frost events and risk assessment. Oecologia 171: 743-760.

Ladinig U, Wagner J. 2009. Dynamics of flower development and vegetative shoot growth in the high mountain plant Saxifraga bryoides L. Flora - Morphology Distribution Functional Ecology of Plants 204: 63-73.

Larl I, Wagner J. 2006. Timing of reproductive and vegetative development in Saxifraga oppositifolia in an alpine and a subnival climate. Plant Biology 8: 155-166.

Leitch IJ, Bennett MD. 2007. Genome size and its uses: the impact of flow cytometry. In: Doležel J, Greilhuber J, Suda J, eds. Flow cytometry with plant cells: analysis of genes, chromosomes and genomes. Weinheim, Germany: Wiley-VCH, 153-176.

Lososová Z, Šmarda P, Chytrý M, Purschke O, Pyšekk P, Sádlo J, Tichý L, Winter M. 2015. Phylogenetic structure of plant species pools reflects habitat age on the geological time scale. Journal of Vegetation Science 26: 1080-1089.

Lubbe FC, Henry HAL. 2019. The cost of depth: frost avoidance trade-off in herbaceous plants. Plant and Soil 444: 213-224.

Meloche ChG, Diggle PK. 2001. Preformation, architectural complexity, and developmental flexibility in Acomastylis rossii (Rosaceae). American Journal of Botany 88: 980-991.

Mori G, Kawabata H, Imanishi H, Sakanishi Y. 1991. Effects of temperature on flower initiation and development in Leucojum aestivum L. and L. autumnale L. Journal of the Japanese Society for Horticultural Science 59: 833-838.

Munguía-Rosas MA, Ollerton J, Parra-Tabla V, De-Nova JA. 2011. Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecology Letters 14: 511-521.

Nitta I, Ohsawa M. 1997. Leaf dynamics and shoot phenology of eleven warm-temperate evergreen broad-leaved trees near their northern limit in central Japan. Plant Ecology 130: 71-88.

Orme D, Freckleton R, Thomas G, Pezoldt T, Fritz S, Isaac N, Pearse W. 2018. caper: comparative analysis of phylogenetics and evolution in R. R package v.1.0.1. Vienna, Austria: Foundation for Statistical Computing. [WWW document] URL https://CRAN.R-project.org/package=caper [accessed 17 April 2018].

Palacio S, Montserrat-Martí G. 2005. Bud morphology and shoot growth dynamics in two species of Mediterranean sub-shrubs co-existing in gypsum outcrops. Annals of Botany 95: 949-958.

Paradis E, Claude J, Strimmer K. 2004. ape: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290.

Pontoppidan M-B, Petersen PM, Philipp M. 2011. For she that hath, to her shall be given … implications of flowering in Anemone nemorosa L. Plant Biology 13: 842-847.

R Core Team. 2016. R: a language and environment for statistical computing. R package v.3.3.2. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL https://www.R-project.org/

Randal WJ. 1952. Interrelations of autecological characteristics of forest herbs. PhD thesis, University of Wisconsin, Madison, WI, USA.

Raunkiaer C. 1934. The life forms of plants and statistical geography. Oxford, UK: Claredon Press.

Rawat DS, Gaur RD. 2004. Floral preformation in alpine plants of the Himalaya. Current Science 86: 1481-1482.

Rosbakh S, Leingartner A, Hoiss B, Krauss J, Steffan-Dewenter I, Poschlod P. 2017. Contrasting effects of extreme drought and snowmelt patterns on mountain plants along an elevation gradient. Frontiers in Plant Science 8: e1478.

Scribailo RW, Tomlinson PB. 1992. Shoot and floral development in Calla palustris (Araceae-Calloideae). International Journal of Plant Science 153: 1-13.

Serebriakov IG. 1949. On the rhythm of seasonal development of flowering plants. 2. Specialization of flower-bearing stems, flower initiation and time of flowering. Byulleten Moskovskogo Obschchestva Ispytateley Prirody, Otdel Biologicheskiy 54: 47-62 [in Russian].

Shefferson RP. 2009. The evolutionary ecology of vegetative dormancy in mature herbaceous perennial plants. Journal of Ecology 97: 1000-1009.

Šmarda P, Knápek O, Březinová A, Horová L, Grulich V, Danihelka J, Veselý P, Šmerda J, Rotreklová O, Bureš P. 2019. Genome sizes and genomic guanine+cytosine (GC) contents of the Czech vascular flora with new estimates for 1700 species. Preslia 91: 117-142.

Sørensen TJ. 1941. Temperature relations and phenology of the northeast Greenland flowering plants. Copenhagen, Denmark: Reitzel.

Šťastná P, Klimešová J, Doležal J. 2012. Altitudinal changes in the growth and allometry of Rumex alpinus. Alpine Botany 122: 35-44.

Veselý P, Bureš P, Šmarda P, Pavlíček T. 2012. Genome size and DNA base composition of geophytes: the mirror of phenology and ecology? Annals of Botany 109: 65-75.

Watson MA, Lu Y. 1999. Timing of shoot senescence and demographic expression in the clonal perennial Podophyllum peltatum (Berberidaceae). Oikos 86: 67-78.

Werger MJA, Huber H. 2006. Tuber size variation and organ preformation constrain growth responses of a spring geophyte. Oecologia 147: 396-405.

Whigham DE. 2004. Ecology of woodland herbs in temperate deciduous forests. Annual Review of Ecology Evolution and Systematics 35: 583-621.

Worley AC, Harder LD. 1999. Consequences of preformation for dynamic resource allocation by a carnivorous herb, Pinguicula vulgaris (Lentibulariaceae). American Journal of Botany 86: 1136-1145.

Genome size is strongly linked to carbohydrate storage and weakly linked to root sprouting ability in herbs

Determinants of interspecific variation in season length of perennial herbs